The Aromatic Plants

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N Natural Products Chemistry & Research DOI: 10.4172/2329-6836.1000227 ISSN: 2329-6836

Review Article Open Access Biosynthetic Factories of Essential Oils: The Aromatic Plants Rafia Rehman1, Muhammad Asif Hanif1, Zahid Mushtaq2, Bereket Mochona3 and Xin Qi4* 1Department of Chemistry, University of Agriculture, Faisalabad, Pakistan 2Department of Biochemistry, University of Agriculture, Faisalabad, Pakistan 3Department of Chemistry, Florida A&M University, Tallahassee, FL, USA 4Department of Medicinal Chemistry, University of Florida, Gainesville, FL, USA

Abstract Essential oils are industrially important natural products of aromatic plants, which are biosynthesized in specialized cells types, such as osmophores, Glandular Trichomes, and ducts and cavities, present on different parts of these plants. In these cells, the essential oils are biosynthesized, accumulated and transferred to the atmosphere by different reported secretion mechanisms. Numerous environmental factors also affect biosynthesis of essential oils and their secretion in the atmosphere. A deep understanding of the entire process is important to improve the yield of biomass of aromatic plants and thus produce large quantities of commercial volatile oils. In this paper, the recent research on types and structure of essential oil-bearing cells, secretion mechanisms, and effect of different environmental factors on essential oil biosynthesis have been comprehensively reviewed. Therefore, this review article will provide new research directions for the researchers working in the field of aromatic plants physiology, essential oil production and many others applications.

Keywords: Aromatic plants cells; Cell organelles; Osmophores; applications [14]. The production of essential oils in plants is generally Glandular trichomes; Environmental factors associated with the presence of specialized secretory structures. After the formation within the plant cells, these oils are also released into the Introduction atmosphere by secreting cells such as osmophores, conical-papillate The aromatic plants have been used by humans as valuable cells, glandular trichomes, ducts, cavities and occasionally non- ethnomedicines for a long time due to the presence of the important specialized cells [11]. The structures of these cells can be characterized secondary metabolites (i.e., essential oils). These essential oils are by state-of-the-art instruments, including light microscopy, scanning important organic molecules because they have natural essence and electron microscopy (SEM), and transmission electron microscopy are biosynthesized in specialized cells of aromatic plants [1-3]. These (TEM) [15-17]. cells have a central role in essential oil biosynthesis, accumulation, and Osmophores secretion into the atmosphere; as a result, they are the natural factories for essential oil synthesis. The study of chemical composition of essential The term osmophore, where “osmo-“ means “odor” and “-phore” oils has revealed that these oils are comprised of highly functionalized means “bearing”, was established in 1962 to describe an enclosed area chemical classes including monoterpenoids, sesquiterpenoids, of floral tissue that is specialized in scent emission. Osmophores, also phenylpropanoids, etc. [4]. called floral fragrance glands, are specialized clusters of cells in flowers, The aromatic plant cells that secrete essential oils are very diverse and are distributed on sepals and petals to attract insect pollinators in morphology, ranging from highly specialized trichomes to non- [15]. Osmophores consist of a multilayered glandular epithelium with specialized cells, osmophores, and secretory cells of petal’s epidermis. homogeneous layers of cells, except in the 18 species of Stanhopea Previous studies have shown that ducts, cavities, secreting trichomes, and Sievekingia, in which osmophores have epidermal cells that are conical-papillate cells, and other essential oils secretory tissues usually morphologically different from the subjacent cells [16,18]. These cells possess specialized cellular structures [5-10]. contain dense cytoplasm, enormous deposits of starch, or other storage compounds within the mesophyll. These deposits are usually missing The pathways of biosynthesis of the essential oils and other in epidermis cells. This generates a distinction between the production aromatic compounds are recognized in these various types of cells. The and the emission layer [18]. granulocrine and eccrine mechanisms are two different mechanisms of secretion, proposed to be responsible for the secretion of essential There has been success in the study of mechanisms of fragrance oils. This fact is supported by studies showing that both mechanisms emission via osmophores. Osmophore cells look similar to the conical- could exist for different compounds and different plants [11,12]. papillate cells that can be found on the whole epidermis of petals in more Furthermore, research shows that different environmental factors than 200 species [19], including Rosa x hybrid (Figure 1), Stanhopea affect the yield and constituents of these essential oils [13]. In this and Sievekingia [16], Galanthus nivalis [17], Araceae, Orchidaceae, and paper, studies conducted on the specialized essential oil-secreting cells, even the model-plant Arabidopsis thaliana (Brassicaceae) [5]. their cellular structure, the secretion pathways, and environmental factors affecting biosynthesis of these oils have been reviewed comprehensively. Comprehensive review of the cellular structure of essential oil-secreting cells has been addressed in this paper to meet *Corresponding author: Xin Qi, Department of Medicinal Chemistry, University of the urgent need to incorporate updated information. Taken together, Florida, Gainesville, FL, USA, Tel: 352-294-5581; E-mail: [email protected] this review will have a high impact on future study of aromatic plants Received May 14, 2016; Accepted May 24, 2016; Published May 31, 2016 as biosynthetic factories of essential oils, granting new opportunities in Citation: Rehman R, Hanif MA, Mushtaq Z, Mochona B, Qi X (2016) Biosynthetic this expanding field. Factories of Essential Oils: The Aromatic Plants. Nat Prod Chem Res 4: 227. doi:10.4172/2329-6836.1000227

Essential Oil-secreting Cells in Aromatic Plants Copyright: © 2016 Rehman R, et al. This is an open-access article distributed Historically, essential oil plants have been valued for their medicinal, under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the culinary, and fragrant properties and possess various biological original author and source are credited.

Nat Prod Chem Res Volume 4 • Issue 4 • 1000227 ISSN: 2329-6836 NPCR, an open access journal Citation: Rehman R, Hanif MA, Mushtaq Z, Mochona B, Qi X (2016) Biosynthetic Factories of Essential Oils: The Aromatic Plants. Nat Prod Chem Res 4: 227. doi:10.4172/2329-6836.1000227

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This conical-papillate shape is known to offer a very large surface found attached to fossil seed fern leaves [31], however, appear to be area for evaporation and participate in the reflection of light. The absent from conifers. Within the angiosperms, apart from hydropotes MIXTA gene, giving rise to the conical shape, has been cloned in and related GTs of some Nymphaeales, GTs are not present in Antirrhinum majus (Scrophulariaceae). Surprisingly, its overexpression Amborella, Nymphaea, Illicium, Trimenia and Austrobaileya [8,32]. in 35S::MIXTA Nicotiana tabacum (Solanaceae) leads to ectopically GTs are often illustrated as randomly spread over surfaces of secreting trichomes on the whole plant, suggesting a relationship plants, although vigilant observations point out that this is usually not between conical-papillate cells and the differentiation of secreting the case. In peppermint, for example, peltate GTs appears more or less trichomes [20]. evenly spaced and is very infrequently found as pairs or clusters. They Cytoplasmic lipid inclusions and plastoglobuli in amyloplasts are are separated from each other by a similar number of epidermal cells, two features presumably associated with fragrance production that but have predictable densities within different regions of a leaf [33]. showed sufficient variation for inclusion here as potentially useful Recent studies have recognized networks of transcription factors that characters. Plastoglobuli are present in the amyloplasts of both species appear to act together as activators or inhibitors of trichome initiation of Sievekingia and most of the species of Stanhopea [16]. In flowers and maturation in protodermal cells [24]. The diversity of secretory of Galanthus nivalis, the osmophores have the structural features of trichomes among the Lamiaceae, Solanaceae and Rosaceaeisisis is polarization of the epidermal cell protoplasts, large cell nuclei, and shown in Figure 2. large vacuoles with heterogeneous contents in the peripheral part of the cells [17]. In Stanhopea graveolens and Cycnoches chlorochilon, the osmophores are positioned in the basal part of the labellum. The area of fragrance emission increased due to the wrinkled surface of the osmophores. The remnants of secretion are noticeable on the surface of the epidermis in S. graveolens, but these are missing in C. chlorochilon [15]. Glandular trichomes Most plants have hairs, called trichomes, on their surface that serve a number of functions ranging from protection against insect pests to heat and moisture conservation [21]. Trichomes occur in plants in a great variety of forms and are sometimes very structurally complex [22]. Two main types of trichomes can be distinguished: non-glandular Figure 1: Environmental electron micrograph of the petal and GTs [23]. Figure 1: Environmental electron micrograph of the petal epidermis of Rosa x hybridaepidermis (Gr. X 600). of Rosa The xessential hybrida oil (Gr. droplets X 600). seem The essentialto gather togetheroil drop due- to GTs (Glandular trichomes) are hairs present on the epidermis and environmentallets seem conditionsto gather intogether the microscope due to chamberenvironmental [11]. conditions have cells that are specific to the biosynthesis and emission of abundant in the microscope chamber [11]. quantities of specific secretory products, such as nectar, mucilage, acyl lipids, digestive enzymes, or essential oils. These secreting trichomes are very numerous and have very different morphologies in the plant kingdom [24]. GTs contains or secretes a mixture of chemicals that have been found to have an enormous array of uses in the pesticide, pharmaceutical, and flavor/fragrance industries. In addition to these industrial uses, GTs on some crop species confer resistance against insect pests [21]. Thus, today there is an increasing interest in understanding the chemistry of glandular trichome exudates and taking advantage of their potential uses [24]. GTs are present in numerous monocotyledons plants, together with the members of the Tradescantia [6], Dioscorea [25], and Sisyrinchium [7]. In the eudicots, GTs are more prevalent and are unique vegetative epidermal features of many families and genera including the members of the Lamiaceae, Asteraceae, Sphaerosepalaceae, Caryophyllaceae, Cucurbitaceae, Fabaceae, Rosaceae, Sapindaceae, Saxifragaceae [24], and Cannabaceae [13]. Metcalfe and Chalk provided a more complete list of the distributions of GTs of various morphological types in dicotyledons [24]. Figure 2: Diversity of secretory trichomes among the Lamiaceae (A, B, C), GTs can be branched or unbranched, sessile, elongated, or short. Solanaceae (D, E) and Rosaceae (F): Environmental electron micrograph of Usually, a group of glandular cells is present at the tip of a stalk of one peltate and capitates glandular trichome of Mentha piperita (A, Gr. x 400). Note the shadow (arrows) of the 8 head-cells before the secretory phase of peltate or more cells in length. Frequently, a thick cuticle layer on the glandular glands. Light micrographs of secretory trichomes of Ajuga reptans (B, Gr. x cells detaches itself from the attached cell wall to form a subcuticular 400) with its thick stalk, Lamium maculatum (C, Gr. x 400) with the subcuticular pocket in which secretions accumulate [6,11,13,26-28]. oil droplet, Lycopersicon esculentum (D, Gr. x 400) with the 4 head-cells, Nicotiana tabacum (E, Gr. x 400) with the sticky secretion (thin arrow) and GTs are widespread in some genera of ferns [29,30] and have been Rosa x hybrida (F, Gr. x 100) with the numerous cells [11].

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Dai et al. presented an integrated “omics” database, TrichOME, to have several big, non-green, spherical plastids differing significantly make possible the study of plant trichomes. A large volume of functional in shape from the leucoplasts of the glandular cells. They also contain omics data is present in the database, and as a result is a precious and comparatively tiny vacuoles, several mitochondria and a comparatively distinctive source for plant trichome research, because the genes large quantity of microbodies [33]. These specialized features were also and metabolites expressed in trichomes are often underrepresented reported for stalk cells of Nepeta racimosa L. and were found to be in regular non-tissue-targeted cDNA libraries. TrichOME is freely associated with the secretory phase of glandular trichome development [46]. available at http://www.planttrichome.org [34]. Role of leucoplasts and microbodies Ducts and cavities Plant glands emitting hydrophobic essential oils and resins share Secreting cells such as ducts and cavities often excrete gum, resin, a number of common features. They frequently enclose amoeboid paste or glue. For example, in conifers, diterpenoid resin acids are leucoplasts that are occasionally bound by an enclosing layer of present in ducts and dissolved in volatile turpentine. Upon injury, periplastic smooth endoplasmic reticulum. Several contacts of the turpentine evaporates, and the resin forms a crystalline mass that plastid and smooth endoplasmic reticulum membrane are observable may trap pathogens and insects [35]. Ducts and cavities are present in [9,13,39,45,47]. different plant families such as Apiaceae [36,37], Compositae [9], or Since the 1960s, leucoplasts have been linked to plant oil secreting Rutaceae [38], Heliantheae [39], and Rubiaceae [40]. Secretory ducts glands and resin-secreting glands and their role in monoterpene and non-GTs also exist in the leaves and stems of Baccharis species [41]. biosynthesis has been well-recognized. Carde et al. comprehensively Surprisingly, numerous plants emit volatile organic compounds described the development, structure and function of plant oil glands (VOCs) by non-specialized cells. For example, in the Brassicaceae, leucoplasts from resin ducts, secretory cavities and GTs [24,48]. The there are no specialized secretory tissues. Nevertheless, it was shown leucoplasts of resin ducts and secretory cavities were found to be very that volatile monoterpenoids and sesquiterpenoids are emitted from analogous to those present in glandular trichomes, although only some the green leaves of these plants directly or after injury. These VOCs of the leucoplasts they examined were from monoterpene-secreting may be emitted for the defense of the plant [42-44]. Only the liverworts trichomes [48]. (Hepatics), in the Bryophytes, contain oil bodies and biosynthesize large In 1983, Gleizes et al. demonstrated that when provided with the amounts of essential oils. Liverwort oil bodies are intracytoplasmic terpenoid precursors IPP (isopentenyl pyrophosphate) and DMAPP secretory structures bound by single membranes that originate from (dimethylallyl pyrophosphate) in vitro, the isolated leucoplasts from the dilatation of endoplasmic reticulum cisternae [10]. secretory cavities of the exocarp of Citrofortunella mitis fruits were Cellular Structure of Volatile Secreting Cells able to synthesize monoterpene hydrocarbons [49]. Then Cheniclet and Carde carried out a large comprehensive study involving 45 Studies show that ducts, cavities, secreting trichomes, conical- species and showed that there is a strong correlation between the papillate cells and other tissues that secret essential oils and volatile presence and volume of leucoplasts in gland cells and the quantity of organic compounds (VOCs) usually contain small vacuoles, dense monoterpenes in the secretion produced by the cells [48]. The study cytoplasms and numerous mitochondria. Leucoplasts, plastoglobules about the morphology of developing leucoplasts in Pinus pinaster resin and unusual figures of reticulum or dictyosomes, like periplastidal ducts revealed that these leucoplasts enlarge continuously to form large reticulum, smooth tubular reticulum, myelin-like lomasoma and complex structures with large central bodies having many deep pockets osmiophilic vesicles or cisternae for example, are also sometimes and small branches, which were all originated from a small number of observed [5-10]. proplastids present in newly-formed gland cells. The large leucoplast The epidermal cells of osmophores have a visibly nonporous and surface in a pine resin duct gland cell was in close contact with covering mainly smooth cuticle, but cuticular blisters are observed. The secretory periplastic endoplasmic reticulum [50]. tissues consist of epidermal cells, numerous layers of small, sub- The microbodies in the cells of the peltate oil hairs ofOriganum epidermal glandular parenchyma, large nuclei, and dense cytoplasms dictamnus (Lamiaceae), the oil cavities of Citrus deliciosa (Rutaceae) with numerous endoplasmic reticulum profiles. Many large idioblasts and the oil ducts of Apium graveolens (Apiaceae) have been studied are observed with phenolic content and/or raphides in the secretory to elucidate their unigue structures. The microbodies appear in the and ground parenchyma. In some parts of the osmophore tissue, cytoplasm of the head cells in the peltate hairs in a significant number lipids almost completely fill the cells. TEM observations [15] indicate during the stage of secretion and are globular to ovoid in shape with the presence of large lipid droplets, mostly close to the outer wall of a 0.4 μm average diameter. These have a single layer of membrane the epidermal cells. In the vacuoles, osmophilic precipitates and small and their matrix consist of a loose specky substance with low electron vesicles are present. The presence of plasmodesmata is common in the density instead of being densely-arranged, fine granules as the typical walls of the epidermis and the adjoining parenchyma. In the cell walls leaf peroxisomes. These microbodies are dispersed and donot form of the osmophore cells, numerous pits with plasmodesmata occur to close links with other cell organelles [51]. take part in symplastic transport of the aroma compounds [5,16,17]. On the basis of ultrastructural, cytochemical and biochemical Multiple of cells are present in the stalks of glandular trichomes. observations on origination of microbodies it has been concluded that They often contain one or more sets of barrier cells that have the microbodies originated from the endoplasmic reticulum [52]. The noticeably impregnated lateral walls. It has been suggested that the particular enzymes involving in the biosynthesis of essential oil have impregnated cell walls permit the stalk cells to control directional been recognized cytochemically in the endoplasmic reticulum matrix transport of metabolites to the glandular cells above [28,45]. Stalk [53]. So, this might provide a reasonable basis of the occurrence of cells of peppermint peltate GTs have strongly impregnated lateral the essential oil-biosynthetic enzymes within the microbodies. The walls, but their ultrastructure suggests additional unknown functions. association of the microbodies with the cytosol of the secretory cells These peppermint cells are metabolically active at emission stage and in the oil glands studied might provide a ground of interpretation for a

Page 4 of 11 possible presence of terpene biosynthetic enzymes in the microbodies. cells can be reconsidered by including the peroxisome as an added Supportive to these interpretations, the appearance of the microbodies isoprenoid biosynthetic compartment [64]. during the stage of essential oil secretion demonstrated their relatively high numbers and divergences from the typical peroxisomes with Secretion Mechanism of Essential Oils respect to their structure and size [13,24,25,28,35]. The transport of essential oils from one region to another Role of the endoplasmic reticulum within the plant cell or to outside the plant body occur by different mechanisms, but the two most significant mechanisms of secretion The suggestion of the role for endoplasmic reticulum-leucoplast include granulocrine and eccrine mechanisms [65,66]. In granulocrine and endoplasmic reticulum-plasma membrane contact sites is mechanisms, vesicles of reverse pinocytosis directly fuse with the persuasive for intracellular transport of terpenoids in the oil gland cells plasma membrane or are surrounded and detached from the cytoplasm of plant. These membrane contact sites are common in plant essential by invaginations of the plasma membranes [64,65]. oil-secreting cells. In many species, the extensive periplastic membrane On the contrary, the eccrine mechanism is the diffusion or active contact sites found surrounding leucoplasts forms numerous clear transport of oil droplets across membranes [65]. These mechanisms are associations between the smooth endoplasmic reticulum and the studied by histochemical methods using Sudan stains, NaDi’s reagent, leucoplasts. Furthermore, previous studies suggest that membrane- Nile blue A and Fluoral Yellow 088 [65-67]. Other stains, such as contact sites are also common between the smooth endoplasmic nitrosophenol for monoterpenes phenols [68] and ferrous thiocyanate reticulum and mitochondria as well as between the cortical smooth for sesquiterpenes [11] are also used occasionally. Such cytochemical endoplasmic reticulum and the plasma membrane [15,18,27,28,47,53]. studies are thus very helpful to locate oil droplets containing terpenes. The physical properties of monoterpenes indicate that intracellular Nevertheless, in numerous electron micrographs, vesicles of essential transfer of secreted monoterpenes could be facilitated by the numerous oils have been precisely located in specialized cells [66]. membrane-contact sites between the smooth endoplasmic reticulum In secretory trichomes, mechanisms of oil secretion have led to a and other organelles. Then these monoterpenes diffuse easily into outer range of hypotheses. In Origanum dictamnus (Lamiaceae) [69], Mentha leaflet lipid membranes [54,55]. Immunocytochemical localization x piperita (Lamiaceae) [33] and Lavandula pinnata (Lamiaceae) [70] experiments provided direct evidence that the enzymes catalysing the the operative secretion mechanisem is eccrine. In Nepeta racemosa first committed steps of monoterpene biosynthesis reside within the (Lamiaceae), Artemisia annua (Apiaceae) [46,71] and Leonotis leonurus stroma of gland cell leucoplasts [53,56]. (Lamiaceae) [72] plasmic membrane budding are involved in secretion whereas in Prostanthera ovalifolia (Lamiaceae) [68] clear granulocrine The role of plastids secretion mechanism is involved. In osmophores, ducts, and cavities, a granulocrine process is most often suspected with observations The plastids of the glandular trichomes, osmophores, secretory of oil droplets often originating not only from plastids, periplastidal cavities, and secretory ducts are often non-pigmented and amoeboid reticulum and smooth reticulum but also sometimes from dictyosomes shaped, have few ribosomes, lack thylakoid membranes, appear to or other organelles [10,38-40,44,73]. associate strongly with the presence of monoterpenes in the secretion product and hence are different from the chloroplast of neighbouring The plant Pterodon pubescens benth is a unique example of the chlorenchyma tissue [48]. The plastids of glandular cells of some plants, involvement of holocrine as well as eccrine and granulocrine processes including the GTs and apical glandular cells of some members such as in the same secretory system, which is not common in other plant the Solanaceae, Asteraceae [57] and Nicotiana tabacum L. [58] contain species. In secretory cavities, due to the presence of oil droplets adjacent functional chloroplasts as well as copious amount of photosynthesis to the plasma membrane of the epithelial cells and in the lumen, an related enzymes. In contrast, the GTs of Artemisia annua L. contain five eccrine secretion mechanism is suggested. In addition, a granulocrine layers of cells, three of which contain well-developed chloroplasts and secretion process is suggested due to the abundance of vesicles filled two of which contain leucoplast-like plastids, suggesting potentially with dense contents in the peripheral cytoplasm and adjacent to the different physiological specializations for the different cell layers plasma membrane. The disruption of the dark epithelial cells followed [27,48]. Similar GTs with cells having chloroplasts and cells containing by the release of their contents into the lumen cavity characterizes a apparent leucoplasts come out to be widespread in the Asteraceae and holocrine secretion process [66]. have been illustrated from Sigesbeckia and Helianthus [59,60]. In the family Pedaliaceae, two secretion mechanisms are reported The role of peroxisomes in long and short trichomes of Ceratotheca triloba. A marked circular area in the upper part of each head cell of the long trichome is provided The studies of different researchers have revealed that the with micropores to secrete the secretory product directly onto the leaf enzymes of biosynthetic pathways of essential oils are present in surface by an eccrine pathway. The short trichomes secretion mode peroxisomes. A study of Sapir-Mir et al. [61] revealed that the two granulocrine and involves two morphologically and histochemically isoforms of IPP(Isopentenyl pyrophosphate) isomerase, catalyzing the distinct vesicle types. One is the Ruthenium Red test positive small isomerization of IPP to DMAPP (Dimethylallyl pyrophosphate), are Golgi-derived vesicles for mucilaginous polysaccharides, and the found in the peroxisomes. Further studies also showed the peroxisomal subsequent type is similar to that of long trichomes and consists of dark localization of the last two enzymes of the mevalonic acid pathway, large microbodies with low extent [66]. including 5-phosphomevalonate kinase and mevalonate 5-diphosphate decarboxylase leading to IPP [62]. This result was emphasized by the In the Leguminosae family, scent-secreting cells are distributed later report, which revealed that using IPP and DMAPP as substrates, a restrictedly on petals of Caesalpinia pulcherrima, Anadenanthera short isoform of farnesyl diphosphate, is also localized to this organelle peregrina, Inga edulis, and Parkia pendula, comprising mesophilic [63]. Hence, the classical compartmentation of isoprenoid biosynthesis osmophores and in a disperse way in Bauhinia rufa, Hymenaea between plastids and cytosol/endoplasmic reticulum within plant courbaril, Erythrostemon gilliesii, Poincianella pluviosa, Pterodon pubescens, Platycyamus regnellii, Mucuna urens, and Tipuana tipu. The

Page 5 of 11 mechanism of emission of essential oil from the petals of these plants In Rosa damascene, the essential oil is present in all parts of is diffuse release [74]. In Rosa x hybrida, changes taking place during flower. Generally, when the petals develop into a cup shape and the maturation of rose petal cells have been studied. Like in other secretory stamens are bright yellow, the essential oil achieves the maximum yield cells, plastoglobules are often observed. Furthermore, at the stage of generally. In the crown petals, the rate of biosynthesis of essential oil is maximal scent emission, tightly whorled structures, supposed to be highest. The composition of rose oil also fluctuates significantly with lipophilic in nature, and other vesicular material of unknown function the developmental stages of flower. This is due to different rates of were observed. These vesicles could be associated with the cell wall and synthesis of different components. In the initial stages of development, putatively concerned with the secretion of petal monoterpenes. It could flowers have more concentration of stearoptene, alpha pinene and well play a role in an eccrine process [75]. myrcene as compared to the important alcohols, citronellol, geraniol, and nerol. The alcohol content quickly increases to about 60% in later Factors Effecting Essential Oil Biosynthesis stages of development [89]. In Salvia sclarea, the essential oil yield Although secondary metabolites in the medicinal and aromatic was less at flowering bud stage, highest at full bloom stage, and then plants are controlled conventionally by their genotypes, their decreased rapidly upon maturation. The oil consisted of linalool (main biosynthesis is strongly affected by factors of the environment, too. constituent), linalyl acetate, β-Humulene, α-cadinene, β-caryophyllene, It means biotic and abiotic environmental factors affect the growth and sclareol, which showed a steady increase in percentage over parameters, essentialoil yield, and constituents of these oils [13]. Some the different stages of maturity, with no significant yield losses at of these factors are reviewed in comprehensive details in the following maturation stage. The yield of essential oil and monoterpenes decreased sections. at full maturity [90]. Developmental stage of the plant The effect of ultraviolet radiations One of the most important factors that affect the essential oil Ultraviolet radiation is an important factor because, in many biosynthesis is the dependence of the synthesis and accumulation of oil cases, it stimulates the production of secondary metabolite. The part on the developmental stage of the related cells, tissues, organs and plants of the ultraviolet daylight spectrum, which is particularly variable and of special attention, is the UV-B band with 280-315 nm. The research as well. The plants containing the leaves as a resource of commercially showed that in two different chemotypes of Mentha spicata, UV-B important essential oil differ in developmental stages of leaves, from radiations caused a 50% increase in essential oil production on a dry- the origin to growth to full maturity tofinally loss through senescence, weight basis in one, while in the other chemotypes, the increase was not are principally vital. A close correlation between leaf development and worth mentioning [91]. oil biosynthesis and accumulation has been demonstrated in many aromatic plants of Lamiaceae family [76-78] and some of Poaceae [79] More detailed research was carried out on the biosynthesis of and Asteraceae [80] plants. essential oil in sweet basil (Ocimum basilicum L.), in which the effect of ultraviolet radiation was of great significance. The effect of UV-B The stage of development also affects the composition of the radiation increased with the plants’ age and was positively different for essential oil. In C. flexuosus, citral, thechief component, reaches its 22 different essential oil components [92]. It was reported in a separate maximum concentration at the twentieth day of development [79]. study that for normal development and filling of oil glands in sweet basil, Salvia offıcinalis possesses camphor which is enhanced in concentration UV-B radiation is needed [93]. Chang et al. studied that irradiating the with leaf expansion [78]. In Japanese mint, the essential oil and main Ocimum basilicum to supplementary UV-B light in the early morning component of the oil, menthol, attain peak concentration at the stage of in a restricted environment in room temperature produced shorter flower bud initiation. But individual leaves show a progressive decrease plants with higher dry mass, more axillary shoots, and thicker leaves in oil percentage with the increase in dry matter and age of the leaf. The [94]. In Mentha piperita, the oil contents were increased to some extent concentration of menthol in oil was increased up to the stage of leaf by UV-B radiation, but the menthol concentration was considerably maturity and then started to decreasewith further aging [81]. decreased as the synthesis of menthone, menthofuran, and menthyl acetate was increased. The stem elongation of plant was significantly In Artemisia annua, the proportion of the major constituent, inhibited, along with changes in leaf area [95]. The application of UV-A artemisia ketone, goes above 50% at the stage of peak flowering [82]. radiation (360 nm) during the day considerably improved the total Studies conducted on M. arvensis [83,84] demonstrated that menthone essential-oil content, especially menthofuran and menthol. The total is in peak concentration in young leaves and menthol in mature leaves. leaf area and total phenols were increased as well. But during the night A similar gradual increase in monoterpene alcohols was also recorded time when this plant was exposed to UV-A radiation, a typical shade- in peppermint with advancement of leaf age [83,85,86]. The effects of avoidance syndrome was produced with elongated stem, decreased leaf the three maturity stages of lemongrass on chemical composition of area, and less essential oil and menthol content [96]. The study of the essential oil and citral contents were studied by Tajidin et al. and it effects of different UV-B radiation (280-315 nm) and photosynthetically was found that maturity stage at harvest influenced essential oil and active radiation (PAR, 400-700 nm) levels and ratios on yield and citral contents of lemongrass [87]. Thyme Origanum( syriacum L.) pattern of essential oil of peppermint showed that during flowering, showed the effect of growth stages such as the pre-flowering stage and the maximum essential oil yield was obtained at high PAR (1150 μmol −2 −1 −2 blooming stage on yield and composition of the essential oil. Total yield m s ) and almost ambient UV-B radiation (0.6 Wm ). The menthol of oil was higher in the plant at blooming stage in comparison with that contents were reduced and menthone contents were increased in the −2 −1 at pre-flowering stage. The higher levels of volatile compounds were absence of UV-B radiation and at low PAR (550 μmol m s ), and hence the oil quality was substantially decreased [97]. noticed during the blooming stage. Exceptions were carvacrol, gamma- terpinene, alpha-terpinene, and para-cymene where higher levels were Cymbopogon flexuosushas also been analyzed to study the effect of found in pre-flowering stage. Unexpectedly, carvacrol as structural supplemental Ulatraviolet-B (sUV-B) radiation on yield and chemical isomer of thymol depicts higher concentration at pre-flowering stage [88]. composition of its essential oil. The exposure to sUV-B radiation

Page 6 of 11 for different intervals of time (15 min, 30 min and 1 hr) showed an gratissimum L., grown under watered and water-stressed field increased percentage of essential oil in aerial parts of the plant. There conditions in full sunlight and natural shade (26.7-44.2% full sunlight) was no significant variation observed in essential oil percentage of conditions were investigated. Plant height and total leaf area of the sub-aerial parts. The analysis of essential oils of aerial parts showed an African basil were decreased more by water stress than by the light or increase in citral percentage in UV treated plants as compared to the shade condition. Shade enhanced essential oil content and water stress control. In sub-aerial parts of sUV-B-treated plants, neral and junipene boosted essential oil content under shade, but reduced oil content were found in higher percentages [98]. under full sunlight. The effects of water stress were only observed in plants in full sunlight. The results demonstrated that African basil will Effect of light quality produce relatively high essential oil yields per plant when grown under The light quality and light intensity can affect the chemical natural shade, regardless of water stress and poor vegetative growth components of plants and percentage of accumulation of the secondary [107]. metabolites in plant tissues. In the aromatic plants, the essential oil Effect of salt stress yield and composition is affected by the quality of electromagnetic radiations [99]. In the leaves of geranium (Pelargonium spp.), the Salt stress is one of the major serious environmental factors biosynthesis of the essential oil is affected by the quality of incident restricting crop production in marginal agricultural soils in many light of different wavelength regions of the spectrum. The irradiation to arid and semi-arid parts of the world. Different aromatic plants show 14 red light caused the biosynthesis of essential oil from CO2 as a primary different effects of salinity stress on yield and composition of essential precursor supplied externally [100]. The research conducted on dill oils produced by them. The main harmful effects of salinity on growth (Anethum graveolens L.) to study the effect of light quality, concerning of plant and yield are attributed to osmotic effect, ion toxicity and different wavelength regions like supplemental red, far-red and blue nutritional imbalance leading to photosynthetic efficiency and stomatal light treatments, and end of the day light treatments, showed no closure [108]. significant differences in the biomass yield of plant. The plants treated A field experiment conducted on three species and four varieties with far red light gave the highest essential oil yield. Consequently, the of basil to evaluate their behavior in saline soil in Egypt showed that plants exposed to 4 hr of red and far red light produced oil containing O. basilicum. Var. Siam queen and O. tenuiflorum were better in plant more phellandrene and less myrisiticin. With an increase in the light height and number of branches per plant, while O. basilicum. Var. level, the growth and essential oil yield increased in dill, and under full genoveser and O. tenuiflorumproduced the highest values in fresh and sunlight it was highest [101,102]. dry weights in both season. O. basilicum. var. Siam queen contained The influence of different wavelengths of lights on biosynthesis of maximum essential oil yield, while the O. basilicum. var. purple ruffles essential oil has also been invetigated in sage and thyme. The exposure variety contained minimum yield of essential oil [109]. The effects of to 45% of full sunlight resulted in the sage plants having peak yield of four levels of salinity on dil showed that mean essential oil yield was essential oil with (+)-thujonone as a major component and camphor in increased with increasing salinity. It was concluded that the dill plant less concentration, as compared to the plants grown under other levels is highly salt-tolerant, and it can perform well under NaCl salinities up of sunlight. In thyme, the highest yield of oil and proportion of thymol to 12 dS/m [110]. and myrecene was obtained in full sunlight [103]. The nine-month-old The results of an experiment on peppermint Mentha( piperita L.) seedlings of Pothomorphe umbellata (Piperaceae) were subjected to showed that an increase in the salinity led to reduced length of stem three shade levels (30%, 50%, 70%) and full sun to estimate the effect of and root, fresh weight of stem and root, dry weight of stem and root, shade on the yield and chemical composition of essential oil leaves. The internodes length, total biomass and essential oil percent and yield. highest essential oil concentration was observed in the plants grown The highest values of growth parameters and essential oil percent and under 30% shade and harvested in the second year of development. yield were observed under the non-salinity condition. The increase in Twenty-six chemical substances were identified, with trans-nerolidolas menthone and the decrease in menthofuran with increasing salinity the predominant substance [104]. level improved the commercial quality of the distilled essential oil Three important Mentha spp., including M. arvensis, M. citrata and [111]. M. cardiac, were grown under short-days, normal-days, or long-days In Mentha pulegium L., the yield and composition and biosynthesis conditions for 60 cycles and were analyzed for growth performance of shoot essential oil was shown to be affected by salt stress. The of plants, biosynthesis of essential oil, and yield and composition of essential oil yield was increased by about 2.75 percent under salt stress, essential oil. Under long-day conditions the species showed improved and the percentage of menthone (the major compound of oil) was also growth, which resulted in early flowering in M. citrata. The short-day affected. Salt stress resulted in considerable changes affecting the size plants revealed the highest rate of biosynthesis of the essential oil, and distribution of trichomes on both sides [112]. The water stress and hence the highest yield of essential oil. The oil composition was enhanced the amount of antioxidant compounds in basil leaf tissues also affected by this photoperiodic treatment [105]. Under different and the highest concentration was observed at an irrigation intensity radiation levels of 23%, 46%, and 100%, Mentha aquatica and Mentha of 25%. More decrease in irrigation level to 12% resulted in reduction x piperita were also grown to analyze the effect of photoperiodic of antioxidant compounds and antioxidant activities of basil extracts modulation in a separate study. In all plants subjected to the lowest [113]. level of radiation, leaf area, stem number, and total dry mass werefound to be reduced. Althoughthe essential oil yield and the percentage of Effect of arbuscular mycorrhizal fungi (AMF) menthol, menthone, linalool, and linalil acetate in this oil were decreased with reduction in radiation levels, there was no observable Arbuscular mycorrhizal fungi (AMF) are certainly a crucial correlation between plant development and essential oil synthesis element of the lower soil system and have a substantial documented [106]. effect on the sustainability and yield of agricultural systems. The first step of colonization of arbuscular mycorrhizal fungi is considered The growth and essential oil yield of African basil, Ocimum

Page 7 of 11 to be the stimulation of synthesis of secondary plant metabolites and manganese sulphates at the tillering time and before intiation of such as flavonoids [114], pathogenesis-related proteins [115], and flowering [128]. phenolics [116] in the roots of the host plant. But the accumulation Japanese mint has been found to require Zn for synthesis and of secondary compounds in the aerial parts of mycorrhizal plants has accumulation of essential oil [129]. The Zn at 0.250 mg/L application been considerable less. In Origanum species, the essential oil yields to Khus-khus and at middle circumference position has given the were found to be enhanced in the presence of arbuscular mycorrhizal maximum total oil % as well as the maximum khusimol and khusinol fungi. The studies on Coriandrum, Anethum and Foeniculum vulgare, oil contents [130]. Zn applied as zinc sulphate (2.5 kg/ha) to palmarosa revealed that arbuscular mycorrhizal fungi root colonization altered herb, in the presence of sufficient nitrogen and phosphate increases the essential oil components, and as a result, the essential oil quality the yield of herb and oil [131]. Two field experiments carried out increased [117,118]. In mycorrhizal Artemisia annua the increased on chamomile showed that in calcareous soils the yield of flower concentration of artemisinin was found to be correlated with ahigher and essential oil increased by foliar application of Fe and Zn. The density of glandular trichome in leaves [119,120]. application of Fe+Zn spray at stages of stem elongation and flowering The experiments performed to compare the effectiveness of two had more beneficial effects on flower dry yield, essential oil percentage arbuscularmycorrhizal fungi, Glomus macrocarpum (GM) and Glomus and essential oil yield as compared with spray at only one stage [132]. fasciculatum (GF), on three accessions of Artemisia annua showed that The experiment performed with peppermint grown under drip the synthesis of plant biomass, dry weight of shoot, nutrient status (P, irrigation system to the west of Nile Delta of Egypt, revealed that Zn and Fe) of shoot, concentration of essential oil, and artemisinin in a concentration of 15 ppm cobalt gave the best fresh and dry herb leaves was considerably enhanced in comparison withnon-inoculated yield and the highest essential oil yield, as well as enhance the uptake plants. The degree of growth, concentration of nutrients, and synthesis of macro (N, P and K) and micro (Mn, Zn and Cu) nutrients. The of secondary metabolites of plants changed with the fungus–plant principal components of oil, including menthone and isomenthone, accession combination. The efficacy Glomusof fasciculatum in increased with decreasing content of L-menthol relatively at the increasing essential oil concentration in shoot was more than that of highest concentration of cobalt. The highest content of L-menthol was Glomus macrocarpum. While in two accessions, GM was more effective obtained at the low level of cobalt as compared to the control and other in enhancing artemisinin concentration than Glomus fasciculatum treatments. Thus, the comparatively high concetration of menthol [121]. These two arbuscular mycorrhizal (AM) fungi also considerably in the peppermint oil implies that in newly reclaimed land in Egypt, enhanced the growth and concentration of essential oil of Foeniculum peppermint essential oil of high commercial value could be successfully vulgare. The inoculation of arbuscularmycorrhizal fungi of plants along produced [133]. Inclusion of molybdenum and copper has led to an with phosphorus fertilizer application considerably increased growth, increased herb and oil yield in well-fertilized plants [89]. phosphorus uptake, and essential oil content of plants in contrast to either of the components used alone [118]. The effects of different amounts of complete fertilizer on the yield, fresh and dry weight, and essential oil composition of Satureja hortensis Effect of fertilizers L. were studied by Alizadeh et al. The results showed that the use of The application of fertilizer usually affects the yield of essential fertilizer increased fresh and dry weight in S. hortensis. The effect of oil by increasingthe yield of biomass of plant in a unit area; however, different amounts of fertilizer on the essential oil composition was very fertilizer also shows the effect in a cultivar-specific manner. In oregano slight and was not significant. But the amounts of some components plants, two pot experiments were done in the seasons of 2006 and 2007 such as carvacrol, γ-terpinene and α-terpinene were varied with to study the effect of different levels of nitrogen fertilizer as ammonium fertilizer application [134]. sulphate on the fresh weight of plant and essential oil. The irrigation of The experiment was conducted by Ahmadian et al. onCuminum plants every seven day and application of 1.2 g nitrogen in each potwas cyminum to study the effects of water stress and application of manure useful in increasing the yield of herb as well as yield of essential oil [122]. on percentage of oil and its main components and yield of these The plantJava citronella had been reported to show a positive response components. Results showed that a relationship exists between the to nitrogen fertilizer with cultivars having herbage content difference by main components of cumin essential oil under water and manure up to 42% and oil yields difference (per hectare) up to 36% at the same application. The effect of water stress and manure were significant on nitrogen levels [122]. Further, variation in herb yield with different essential oil and its constituents. The highest amount of cumin aldehyde types of urea used on the same cultivar has also been demonstrated and ρ-cymene and the lowest of β-pinene, γ-terpinene, and α-pinene [123]. In lemongrass, nitrogen application has been found to influence were obtained with manure treatment and three times irrigation [135]. the citral content in oil, but the potassium requirement of lemongrass sometimes exceeds the nitrogen requirement required to produce best Concluding Remarks and Perspectives oil yield [124]. In Rosa damascena, at bud development stage better The aromatic plant cells are impotant natural biosynthetic factories flower and oil yield has been found to be associated with levels of NPK of essential oils with different morphologies, which are present on in leaves, and in many countries rose flower yield has been enhanced different parts of aromatic plants where these oils are biosynthesized, with nitrogen application [125]. accumulate and hence reach the atmosphere by different reported Manganese has been found to be the most valuable single secretion mechanisms. The research reviewed in this paper showed micronutrient that increases the yield of essential oil. In the geranium, that different cell organelles within the plant cells play an important the application of magnesium often increases herb yield but oil role in the entire process from the biosynthesis of essential oil to their concentration or composition has no significant influence [126]. In secretion into the atmosphere by granulocrine or eccrine mechanisms C. winterianus, chlorosis is produced in leaves due to iron deficiency, or both, but their exact mechanism of action during all these processes which reduces herb production and yield. However, their oil contents still needs further exploration. There are many environmental factors are not strongly affected [127]. In palmarosa, both herbage and oil that influence these natural processes of essential oil biosynthesis, their have been found to significantly increase with the application of ferric accumulation and secretion into the atmosphere. We have summarized

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